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Cirral Activity and Feeding in the Barnacle Balanus Perforatus Bruguière (Balanidae), With Comments on the Evolution of Feeding Mechanisms in Thoracican Cirripedes

D. T. Anderson
Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences
Vol. 291, No. 1053 (Apr. 27, 1981), pp. 411-449
Published by: Royal Society
Stable URL: http://www.jstor.org/stable/2395434
Page Count: 39
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Cirral Activity and Feeding in the Barnacle Balanus Perforatus Bruguière (Balanidae), With Comments on the Evolution of Feeding Mechanisms in Thoracican Cirripedes
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Abstract

Earlier studies of rhythmic cirral activity in balanid barnacles have assumed the monophyletic nature of Darwin's Balanidae (s.l.) and a similar performance of normal and fast beat among species in this group. Recent taxonomic revisions of the Balanomorpha have raised the possibility that rhythmic cirral activity evolved polyphyletically at least twice in the Archaeobalanidae (Elminius modestus and Semibalanus balanoides), as well as in the Balanidae (s.s.). Differences in food intake tend to support this hypothesis. B. perforatus has a mode of cirral beating different from that of other species of Balanus (s.s.). Instead of normal and fast beat, B. perforatus exhibits a characteristic action over the whole range of 2-24 beats per 10 s. At all rates, the operculum is held open and the cirri are extended and withdrawn from the mantle cavity during beating. Cirral extension is less at faster rates than at slower rates. While the cirral action is effective in the capture of small planktonic prey such as nauplii, the major emphasis is on pumping a powerful current of water through the mantle cavity. In contrast to other species of Balanus, the volume of water pumped through the mantle cavity increases as the rate of beating increases. An average-sized B. perforatus beating at a fast rate passes water through the mantle cavity at a rate greater than 1 l/h. The action of the maxillipeds and mouthparts in captorial planktivory in B. perforatus is similar to that of other extension feeding and rhythmic feeding balanomorphs. A filtratory action of the large, setose maxillipeds is correlated with the production and flow of the mantle current. At slower rates of beat, up to 9 per 10 s, the main determinant of the rate of beating is the duration of the pause in the withdrawn position. At faster rates of beat, this pause becomes negligible and the main determinant of the rate of beating is the speed of movement of the body during each beat cycle. These two factors, the pause duration and the speed of body movement, appear to be controlled by independent but coordinated neural mechanisms. The evolution of rhythmic cirral beating in balanoids has been mainly of the action of these neural mechanisms in controlling a skeleto-muscular system similar to that of non-rhythmic, extension-feeding balanomorphs. Such an evolution could have occurred more than once. In the absence of detailed information on the relationship between cirral action, body movements, mantle current production and food capture in other balanoid species, the question of whether the rhythmic cirral activity of balanoids has had a monophyletic or a polyphyletic origin from an extension-feeding ancestry cannot be firmly answered at the present time. Similarities have been emphasized in the past, but clear differences exist. Elminius modestus emphasizes fast beat and is a planktivore. Semibalanus balanoides performs both normal beat and fast beat and combines planktivory with supplementary filter feeding. Among the Balanidae (s.s), B. perforatus has a unique rhythmic cirral action and is highly adapted as a current-producing filter feeder. Balanus nubilus appears to have independently evolved a similar pumping-filtering action, but has not been studied in detail. Other `groups' within the genus Balanus variously emphasize rhythmic planktivory or a combination of planktivory and filtration. None of these, on present evidence, could have shared an evolution of rhythmic beating with B. perforatus. The hypothesis that rhythmic cirral activity has evolved polyphyletically in the Archaeobalanidae and Balanidae can therefore be extended to a polyphyletic origin of rhythmic cirral activity among the various groups of the genus Balanus (s.s.). The powerful development of the three pairs of scutal and tergal depressor muscles in B. perforatus, shared by other large balanoid species (e.g. Chirona hameri, Balanus nubilus), is not functionally related to the performance of rhythmic beating or powerful pumping. These muscles function in protective closure of the operculum and in producing a protective rotary action of the closed operculum.

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